Introduction

The genus Garcinia L. is part of the family Clusiaceae which, in its present circumscription (Stevens 2007), is subdivided into two sub-families: Kielmeyeroideae Engl., which includes the African genera Mammea, Endodesmia, Lebrunia and Calophyllum, and Clusioideae Engl. with the African genera Allanblackia, Garcinia, Pentadesma and Symphonia. All but one of these genera (Lebrunia) are present in the Lower Guinea phytogeographical region (western Central Africa; White 1979). Unfortunately, the delimitation of the family and its subdivision have not settled down yet (Stevens 2007, Sweeney 2008, APG III 2009).

Most authors now agree upon a broad concept of Garcinia, including the former genera Rheedia L. and Ochrocarpos Thouars, as well as the small genera Pentaphalangium Warb. and Tripetalum Schumann. One might also merge the genus Allanblackia with Garcinia (Sweeney 2008, Ruhfel et al. 2011), because the first seems phylogenetically nested within the latter, although the support for that is not very strong yet. Moreover, even when the nested position of Allanblackia is confirmed by future studies, regarding the large morphological differences between the latter two genera and hence the comparatively long length of the branch leading to Allanblackia, it will be preferable to accept Garcinia as a natural though paraphyletic genus (Sosef 1997, Brummitt and Sosef 1998).

Amongst the African genera, Garcinia is characterized by the dioecism of its species and hence its unisexual flowers (or at least functionally so, see also Dunthorn (2004) for a study of the situation in Mammea), the presence of a foveola at the base of the petiole (an excavation with an extension resembling a ligule), the peltate stigma, the ovary with a single apical ovule per locule and the berry-like fruit.

Garcinia contains approximately 260 species which are mainly confined to the tropics (Jones 1980, Stevens 2007). Over the centuries, these have been accommodated into many sections, which have been reduced to a total of 14 in an unpublished thesis by Jones (1980). Her view has been largely confirmed by recent molecular work (Sweeney 2008). In Africa, including Madagascar, representatives of six of these sections can be found.

In Lower Guinea (roughly comprising the forested regions in Cameroon, Equatorial Guinea, Gabon, the south-west of the Republic of the Congo, Cabinda (Angola) and the southwest of the Democratic Republic of the Congo; White 1979), and in fact in the whole of the African rain forest region, Garcinia spp. form an important component of the lower strata of dense lowland to submontane rain forests, where they often occur gregariously (Achoundong 1995, Guedje et al. 2002, Thomas et al. 2003, Sosef et al. 2004, Senterre 2005, Gonmadje et al. 2011, Dauby 2012). In Central Africa, some species are also well-known among local populations due to their various medicinal properties (Guedje and Fankap 2001, and see the PROTA website at http://www.protaafrica.org ).

The presence of high numbers of sympatric Garcinia species in almost every tropical region (Ashton 1988, Sweeney 2008) may well have led to a situation where the genus received comparatively little attention from taxonomists because of its supposed complexity. This has resulted in an unsatisfying situation where taxonomic treatments have often only been focussing on a particular region (in Floras for example) and as a result contain various contradictions and errors. This obviously further feeding the idea that Garcinia is a complex and ‘difficult’ genus. Plant collectors, but also foresters, ecologists, etc., are often satisfied when they have concluded that their specimen belongs to the genus Garcinia and when they try to identify their material down to an individual species, they are bound to make many errors due to the unresolved taxonomic backbone.

In tropical Africa, the Clusiaceae (often in their old concept of Guttiferae) have been treated for West Africa (Hutchinson et al. 1954), the Congo Basin region (Bamps 1970a), East Africa (Bamps et al. 1978), and the Zambesian region (Robson 1960). However, no treatment exists yet for the notoriously richest Lower Guinean region (Sosef 1996, Küper et al. 2004). Many West African species extend their range to the east into Lower Guinea while many East and Central African ones do so to the west. Combined with a comparatively high local endemism in Lower Guinea, possibly caused by the presence of Pleistocene rain forest refugia (Sosef 1994, 1996, Linder 2001), this area counts as a diversity hotspot for many angiosperm families (Beentje et al. 1994, Barthlott et al. 1996, Küper et al. 2004, Linder et al. 2005). Besides that, it is also the region where taxonomic views and treatments of ‘West’ and ‘East’ meet and not seldom appear to disagree. During the preparation of a treatment of the Clusiaceae for the revitalized Flore du Gabon (Sosef and Florence 2007), several of thesetaxonomic ‘problems’ within Garcinia were tackled, and it was decided to slightly broaden the scope of that study. The resulting present article clarifies the confusing taxonomy amongst several African members of the sections Xanthochymus (Roxb.) Pierre and Tagmanthera Pierre, describes two interesting new species from Gabon, provides an identification key to the Garcinia’s within thehigh diversity region of Lower Guinea, and hopes to draw attention to the need of more elaborate taxonomic studies in Garcinia.

Materials and methods

The authors studied the available Garcinia material in BM, BR, BRLU, K, L, LBV, MO, P and WAG (herbarium abbreviations follow Index Herbariorum, http://sweetgum.nybg.org/ih ). Additional material was consulted through the JSTOR Plant Science website (http://plants.jstor.org ). In 2008 and 2009, during tree plot inventories and general collecting undertaken in Gabon, the second author collected numerous Garcinia specimens and made many useful field observations.

The conservation status of the two new species was assessed using the IUCN (2001) category criteria. Extent of occurrence and area of occupancy were estimated using Arcview 3.3 and Conservation assessment tools (Moat 2007).

The Garcinia quadrifaria complex On the correct authors of the name Garcinia quadrifaria

The species now known as Garcinia quadrifaria was first described by Oliver (1868: 168) as Xanthochymus ? quadrifarius. It was transferred to Garcinia by Pierre (1883: 4) who seems to credit Baillon (1877: 404) for the name and also cites Oliver (1868: 168). Many sources (including IPNI, (http://www.ipni.org ), Tropicos (http://www.tropicos.org ), etc.) refer to Garcinia quadrifaria with Baill. or Baill. ex Pierre as the authors of this combination. Actually, Baillon (1877) only states that Xanthochymus should be united with Garcinia, and refers to Oliver (1868), but does not make any new combinations. Therefore, the correct author combination for Garcinia quadrifaria is (Oliv.) Pierre.

On the distinction between Garcinia quadrifaria and related species

The species Garcinia quadrifaria belongs to the section Xanthochymus, characterized mainly by having staminal bundles with filaments only partly fused and globose anthers (Jones 1980). Garcinia quadrifaria shows several quite striking characters. Most obvious are the quadrangular and narrowly though distinctly winged twigs, the usually terminal inflorescence composed of a simple and short rachis set by 4 rows of overlapping scale-like bracts (somewhat reminiscent of an inflorescence of a Gnetum species), the 5-merous flowers, a fruit with a verrucose exocarp and white latex. It shares these features with the following, until recently still recognized, species: Garcinia chromocarpa Engl., Garcinia gnetoides Hutch. & Dalziel, Garcinia granulata Hutch. & Dalziel and Garcinia le-testui Pellegr. In the past, two more species names, Garcinia parva Spirlet and Garcinia echirensis Pellegr., have been treated as synonyms of Garcinia chromocarpa (Bamps, 1970a, 1970b).

After careful examination of the characters of Garcinia quadrifaria and Garcinia chromocarpa, we have come to the conclusion that the only distinction between the two is the minute puberulence on the bracts, pedicels and fruits of Garcinia chromocarpa, where those of Garcinia quadrifaria are glabrous. Although at first glance there might be a geographical distinction, Garcinia chromocarpa in the Congo Basin, west to Gabon and Cameroun (Bamps 1970c), and Garcinia quadrifaria in W.-Africa east to Cameroon and Gabon, this could not be upheld because of the presence of true Garcinia quadrifaria in eastern DR Congo (North Kivu: Léonard 2337; Kivu: Gutzwiller 1868) and true Garcinia chromocarpa in Ivory Coast (Breteler 6126, J.J. de Wilde & Leeuwenberg 3442). Also, when studying the literature (Engler 1908, Pellegrin 1959, Bamps 1970a, 1970b) one might conclude that Garcinia chromocarpa has 3-locular ovaries and 3-lobed stigmas, while Garcinia quadrifaria would have 2-locular ones bearing 2-lobed stigmas. Although indeed all true (glabrous) Garcinia quadrifaria specimens studied had 2-lobed stigmas, various true (puberulent) Garcinia chromocarpa ones with 2-lobed stigmas (D.W.Thomas 4874, Walters & Niangadouma 1264, White 767and others) were observed. Finally, from the literature it seems that flowers of Garcinia chromocarpa may have shorter pedicels than those of Garcinia quadrifaria. Again, after proper examination of all the material available this turns out to be incorrect.

We therefore conclude that since the differences between the two taxa are minimal, they cannot be upheld as different species. We do, however, want to distinguish them, and the level of variety seems most appropriate since there is no geographical separation. Because the name Garcinia quadrifaria has priority over Garcinia chromocarpa, this leads to the following new combination:

On the status of Garcinia densivenia and Garcinia zenkeri

Two more species of the section Xanthochymus were described by Engler (1908): Garcinia densivenia and Garcinia zenkeri. The firstwas based on two collections from Cameroon: Zenker 2397 (with flowers) and Zenker 2547(with fruits). The angular twigs and coriaceous leaves are reminiscent of Garcinia quadrifaria. However, the fruit wall is smooth (not verrucose) and the inflorescence is both terminal and axillary and composed of bundles of very short racemes (up to 10 mm). Occasionally the inflorescence is composed of a branched raceme. In our view, this renders the taxon sufficiently distinct to recognize it at species level. To date, no lectotype has been chosen from among the two syntypes, and because the fruit character is the most striking distinction, the best choice would be Zenker 2547. With the duplicate at B lost, we propose to select the duplicate at G, which seems to have the finest fruits, as the lectotype.

Garcinia zenkeri was also based on two Zenkercollections from Cameroon: Zenker 1120 (with flowers) and Zenker 3247(with fruits). According to the African Plants Database (http://www.ville-ge.ch/musinfo/bd/cjb/africa ), Garcinia zenkeri would be a synonym of Garcinia quadrifaria. This view is probably based upon Pellegrin (1959), who only cites the first syntype. Studying material of both syntype collections (especially the first with numerous duplicates in various herbaria), we indeed confirm the presence of angular twigs and coriaceous leaves which point to Garcinia quadrifaria. However, we also observe the presence of inflorescences composed of bundles of short racemes, often axillarily positioned, just as in Garcinia densivenia. The only duplicate of Zenker 3247 (the syntype with fruits)available to us is sterile, and so we were unable to verify whether the fruit wall is smooth as in Garcinia densivenia. On the other hand, Engler l.c. does not mention a verrucose structure of the fruit wall, a feature we believe he would certainly not have missed. We therefore render it most likely that the fruit he observed had a smooth wall. In all, we conclude that Garcinia zenkeri and Garcinia densivenia are synonyms. Both being published in the same publication, we may choose one of the names as being the valid one, and we have picked Garcinia densivenia because the type material is better, showing all diagnostic features. Garcinia zenkeri also needs a lectotypification, for which we have taken Zenker 1120.Although all duplicates we have seen lack flowers, it is by far the most widely distributed collection. Since, again, the material at B was lost and that at G seems the best among the remaining duplicates available, we have chosen that to be the lectotype. The above leads to the following situation:

Garcinia densivenia Engl., Bot. Jahrb. Syst. 40: 563 (1908). ‒ LECTOTYPE (designated here): CAMEROON. Bipinde, Urwaltgebiet, 1903. Zenker 2547(G!, barcode G00018874; isotype BR!, GOET!, K!, M!, P!, WAG!).

Heterotypic synonym:

Garcinia zenkeri Engl., Bot. Jahrb. Syst. 40: 566 (1908), syn. nov. ‒ LECTOTYPE (designated here): CAMEROON: Bipinde, Urwaltgebiet, 1896, Zenker 1120(G!, barcode G00018871; isotype BM!, GOET!, K!, M!, P!, S!, WAG!).

The material now identified as Garcinia densivenia, shows a remarkable variation in the distinctiveness of the tertiary venation. In the type as well as the paratype collection this venation is indeed, as the name indicates, strikingly dense and prominent. However, in most of the remaining material we observed a large continuous variation towards leaves where the tertiary venation was even hardly visible. Because otherwise, the material is quite uniform, we assume this character to be highly variable within the species, and possibly also depending on the way in which the material was treated and dried after collecting.

A second remarkable variation was observed in the shape of the fruits. These can be subglobose to distinctly 5-lobed and ‘pumpkin-like’. The lobed feature was even already mentioned by Engler in his protologue: “Baccae ….. leviter 5-lobae…..” and “schwach 5 lappigen Früchte…..”. However, again, we found no other characters to correlate with this feature. Moreover, the label of Bos 3639 specifically mentions that the shape of the fruits he collected are “globose to shallowly 5-lobed and resembling a pumpkin”. We thus assume that these observations also illustrate within-species variation, and might be related to the number of seeds that develop within a single fruit.

The Garcinia afzelii complex

The section Tragmanthera is characterized by 4-merous flowers and staminal bundles that are completely fused carrying a row of ellipsoid anthers at their tip (Jones 1980). Four of its species, Garcinia afzelii Engl., Garcinia brevipedicellata (Bak.f.) Hutch. & Dalziel, Garcinia lujae De Wild. and Garcinia mannii Oliv., are closely related because they share a unique feature: the presence of anthers with locellate (septate) thecae. After studying the material, we noticed it is fairly easy to split it into two groups based on a leaf venation character: 1) Garcinia afzelii and Garcinia brevipedicellata having leaves with the lateral veins (3-)4-11 mm apart and gradually but distinctly curving up towards the margin and eventually running almost parallel to it, and 2) Garcinia lujae and Garcinia mannii with dense lateral veins, only 1-2(-3) mm apart, that run almost straight to the margin, or curving up just before it, where they join up in a blunt angle with an intramarginal vein running just inside of (at 0.5-1 mm) the actual margin.

Bamps (1970b) already noticed that the latter two species are very closely related. The only remaining differences we could find is the colour of the petals (red to deep orange or sometimes yellow in Garcinia mannii and always yellow in Garcinia lujae) and the length of the staminal bundles (as long as the pistillode in Garcinia mannii and clearly overtopping the pistillode in Garcinia lujae). Although these distinctions are weak, there is no geographical overlap between the two taxa, Garcinia lujae in the Democratic Republic of the Congo and Garcinia mannii from southern Nigeria to Gabon, which made us decide to uphold them at species level, but further investigations are needed.

However, we could not find any clear difference between the remaining two species, Garcinia afzelii and Garcinia brevipedicellata. Hutchinson et al. (1954) give the density of the lateral veins (more dense in Garcinia afzelii) as the only difference, but we have clearly observed this feature to be variable, even within a single specimen. Also, the name of Garcinia brevipedicellata suggests it has short pedicels (although this taxon was originally described as a variety of Garcinia mannii and so this would be a difference with that taxon), but again, those in Garcinia afzelii are quite variable and we observed a continuous variation. Finally, there might be a difference in flower colour, since the petals of Garcinia afzellii are reported to be yellow to pale green, while label data indicates the flowers of Garcinia brevipedicellata are “yellow with a red centre”. The latter observation is indeed correct, because the petals are yellow and the pistillode or ovary has an orange to red colour. Both species have staminal bundles that are longer than the ovary. So, none of the presumed diagnostic characters can be confirmed and we conclude that both names refer to the same species. Since Garcinia afzelii is the older one, that is the accepted name for the taxon.

Finally, the status of the name Garcinia antidysenterica A.Chev. is unclear. At present, it is regarded as a synonym of Garcinia afzelii (Hutchinson et al. 1954, Pellegrin 1959, African Plants Database at http://www.ville-ge.ch/musinfo/bd/cjb/africa ). The protologue text provides information on three collecting localities referring to Chevalier’s own specimens: “entre Nze et Danané”, “entre le Morénou et l’Indénie” and “bassin du moyen Comoé”. No holotype is designated, but the protologue is accompanied by a photo of one of the sheets: Chevalier 21200, collected at “Danané”, and so this seems to be the most logical choice for the lectotype. However, this collection (duplicates at P and K) turns out to be Garcinia epunctata Stapf, as was already discovered by Bamps (1969: 364). While the protologue clearly states that the anthers have locellate thecae, those of Garcinia epunctata and hence of Chevalier 21200 are not. Therefore, choosing the latter collection as the holotype should be avoided, following Article 9.17 of the Code (McNeil et al. 2006; lectotype in serious conflict with the protologue while other elements are available). Chevalier (1920) provides a list of specimens which according to him belong to Garcinia antidysenterica. The only other collection that carries one of the remaining two localities, “vallée du Moyen-Comoé”, is Chevalier 22571. Therefore, this seems the most obvious choice for the lectotype. It has at least three duplicates (BR, K (2x) and P) and the specimen at P should be regarded as the most original material. At least the BR and K duplicate carry an original label with the name Garcinia antidysenterica A.Chev. (The P material was seen at an early stage of the project, but due to the closure of the Paris herbarium the exact label data could not be checked.)

The above now leads to the following situation:

Garcinia afzelii Engl., Bot. Jahrb. Syst. 40: 570 (1908).

Heterotypic synonyms:

Garcinia antidysenterica A.Chev., Vég. ut. Afr. trop. franc. 6: 445, fig. 52 (1911). ‒ LECTOTYPE (designated here): IVORY COAST: vallée du Moyen-Comoé, entre Yabrouakrou et Tingouéla, 13 décembre 1909, Chevalier 22571 (P!; isotype BR!, K!).

Garcinia mannii Oliv. var. brevipedicellata Bak.f., in Rendle et al., Cat. pl. Oban : 8 (1913). – Garcinia brevipedicellata (Bak.f.) Hutch. & Dalziel, Fl. West trop. Afr., ed. 1, 1(1): 237 (1927), syn. nov.

Within the section Tragmanthera some taxonomic questions remain to be solved, for example the distinction between the non-locellate species such as Garcinia epunctata Stapf and Garcinia preussii Engl., and the status of several other names now regarded as their synonyms. For now, we maintain the present status quo, just signalizing the need for a more in-depth study.

Two new endemic Garcinia species from Gabon

During the preparation of the Clusiaceae treatment for Flore du Gabon, material belonging to two new species turned up. Both are endemic to this country that has a plant endemism rate of ca. 11% (Sosef et al. 2006). Gabon is notoriously rich in species (see above), especially its lowland rain forest is reputedly the most species-rich in tropical Africa (Breteler 1990, Linder et al. 2005, Reitsma 1988) and novelties are still regularly discovered (Bissiengou and Sosef 2008, Ntore et al. 2010, Walters et al. 2011).

Key to the Lower Guinean species of Garcinia

For most of the continental tropical African regions, an identification key to the species of Garcinia exists: Hutchinson et al. (1954) for West Africa, Bamps (1970a) for Central Africa, Bamps et al. (1978) for East Africa, and Robson (1961) for the Zambesian region. The lack of such a key for the notoriously species-rich Lower Guinean region has hindered proper identification of specimens; a shortcoming we hope to overcome by providing the key below.

Remaining insufficiently known species